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Randomized Controlled Trial
. 2014 Dec 1:145:77-86.
doi: 10.1016/j.drugalcdep.2014.09.013. Epub 2014 Nov 4.

Altered neural correlates of reward and loss processing during simulated slot-machine fMRI in pathological gambling and cocaine dependence

Patrick D Worhunsky  1 , Robert T Malison  2 , Robert D Rogers  3 , Marc N Potenza  4
Affiliations
Randomized Controlled Trial

Altered neural correlates of reward and loss processing during simulated slot-machine fMRI in pathological gambling and cocaine dependence

Patrick D Worhunsky et al. Drug Alcohol Depend. .

Abstract

Background: Individuals with gambling or substance-use disorders exhibit similar functional alterations in reward circuitry suggestive of a shared underlying vulnerability in addictive disorders. Additional research into common and unique alterations in reward-processing in substance-related and non-substance-related addictions may identify neural factors that could be targeted in treatment development for these disorders.

Methods: To investigate contextual reward-processing in pathological gambling, a slot-machine fMRI task was performed by three groups (with pathological gambling, cocaine dependence and neither disorder; N = 24 each) to determine the extent to which two groups with addictions (non-substance-related and substance-related) showed similarities and differences with respect to each other and a non-addicted group during anticipatory periods and following the delivery of winning, losing and 'near-miss' outcomes.

Results: Individuals with pathological gambling or cocaine dependence compared to those with neither disorder exhibited exaggerated anticipatory activity in mesolimbic and ventrocortical regions, with pathological-gambling participants displaying greater positive possible-reward anticipation and cocaine-dependent participants displaying more negative certain-loss anticipation. Neither clinical sample exhibited medial frontal or striatal responses that were observed following near-miss outcomes in healthy comparison participants.

Conclusions: Alterations in anticipatory processing may be sensitive to the valence of rewards and content-disorder-specific. Common and unique findings in pathological gambling and cocaine dependence with respect to anticipatory reward and near-miss loss processing suggest shared and unique elements that might be targeted through behavioral or pharmacological interventions in the treatment of addictions.

Keywords: Addiction; Cocaine dependence; Near-miss; Pathological gambling; fMRI.

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Conflict of interest statement

Conflict of Interest. The authors report no conflicts of interest with respect to the content of this manuscript. Dr. Potenza has received financial support or compensation for the following: Dr. Potenza has consulted for and advised Boehringer Ingelheim, Ironwood, Lundbeck and iNSYS; has consulted for and has financial interests in Somaxon; has received research support from Mohegan Sun Casino, the National Center for Responsible Gaming, Forest Laboratories, Ortho-McNeil, Oy-Control/Biotie, Psyadon, Glaxo-SmithKline, the National Institutes of Health and Veteran’s Administration; has participated in surveys, mailings or telephone consultations related to drug addiction, impulse control disorders or other health topics; has consulted for law offices and the federal public defender’s office in issues related to impulse control disorders; provides clinical care in the Connecticut Department of Mental Health and Addiction Services Problem Gambling Services Program; has performed grant reviews for the National Institutes of Health and other agencies; has guest-edited journal sections; has given academic lectures in grand rounds, CME events and other clinical or scientific venues; and has generated books or book chapters for publishers of mental health texts.

Figures

Figure 1
Figure 1
Simulated slot-machine task design and example outcome types.
Figure 2
Figure 2
Reward-receipt processing. Whole-brain, cluster corrected (PFWE<0.05) responses to slot-machine winning outcomes (e.g., AAA) across participants
Figure 3
Figure 3
Anticipatory processing. Average anticipatory whole-brain response across all participants (a) at cluster-corrected (PFWE<0.05) threshold while watching final reels spin while the first two reels display matching symbols (e.g., AA?; indicating potential win anticipation) as compared to unmatched symbols (e.g., AB?; indicating certain-loss anticipation). Group differences in anticipatory activity (b) at whole-brain cluster-corrected (red) and uncorrected (blue) thresholds. Regional BOLD signal differences between groups in the right striatum during reward-anticipation are shown in (c). All error bars indicate standard error. Abbreviations: HC, healthy comparison; PG, pathological-gambling; CD, cocaine-dependent; u, arbitrary units. * P<0.05
Figure 4
Figure 4
Non-sequential near-miss processing. Average whole-brain response in response to non-sequential misses (e.g., ABB/ABA) as compared to full-loss outcomes (e.g., ABC) across all participants (a) at cluster-corrected (PFWE<0.05) threshold. Group differences in spatial near-miss activity in these certain-loss outcomes (b) did not survive cluster-correction thresholds, but are displayed at uncorrected (blue) cluster threshold of P<0.05. Average regional BOLD signal differences between groups in the ventromedial prefrontal cortex (PFC) are shown in (c). All error bars indicate standard error. Abbreviations: HC, healthy comparison; PG, pathological-gambling; CD, cocaine-dependent; u, arbitrary units. * P<0.05
Figure 5
Figure 5
Sequential near-miss processing. Average whole-brain response in response to sequential misses (e.g., AAB) as compared to second-reel unmatched (e.g., AB), losing events across all participants (a) at cluster-corrected (PFWE<0.05) threshold. Group differences in temporal near-miss activity in these notification of loss events (b) did not survive cluster-correction thresholds, but are displayed at uncorrected (blue) cluster threshold of P<0.05. Regional BOLD signal differences between groups in the right ventral striatum are displayed in (c). All error bars indicate standard error. Abbreviations: HC, healthy comparison; PG, pathological-gambling; CD, cocaine-dependent; u, arbitrary units. * P<0.05
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